Alien plant species with a wider global distribution are better able to capitalize on increased resource availability
Wayne Dawson1,2, RudolfP. Rohr 3,4, Mark van Kleunen1,2 and Markus Fischerl
Ilnsritute for Plant Sciences, University of Bern, Altenbergrain 21. Bern 3013. Switzerland: 2Ecology, Depanment of Biology, University of Konstanz, Universitiitsstrasse 10, D 78464 Konstanz, Germany; 3Ecology and Evolution. Department of Biology. University of Fribourg. Chemin du Musee 10, Fribourg 1700, Switzerland; 4Integrative Ecology Group, Estacion Biologica de Don.na. CSIC. Cl Americo Vespucio sin. E-41092 Sevilla. Spain
Summary Author of correspondence:
Wayne Dawson Tel: +497531882116
Email: wayne.dawson@uni-konstanz.de
• A high ability of alien plant species to capitalize on increases in resource availability has been suggested as an explanation for being globally successful. Here, we tested this hypothesis meta-analytically using existing data from experiments manipulating plant resources (light, water and nutrients).
New Phytologist (2012) 194: 859-867 doi: 10.1111/j.1469-8137.2012.04104.x
• From these studies we extracted the response to resource increase of biomass, as an indica- tor of plant performance, and the responses of two traits related to resource capture: root:
shoot ratio and specific leaf area (SLA). For 211 species recorded in the Global Compendium of Weeds, we assessed the relationship between effect sizes from such studies and the num- ber of global regions where a species was established.
Key words: exotic, fitness, life history, naturalization, phenotypic plasticity.
• We found that globally widespread species exhibited greater biomass responses to increases in resources overall, compared to less widespread species. Root: shoot ratio and SLA responses to increased resource availability were not related to species global distribution.
• In general, globally widespread alien plant species were better able to capitalize on increased availability of resources, through achieving increased growth and biomass accumu- lation, while greater plasticity of key resource-capture traits per se did not appear to be related to greater success.
Introduction
The ability of plants to increase performance by taking advan- tage of free resources may depend on plasticity of functional traits, in particular specific leaf area (SLA) and root: shoot ratio (Nicotra et aI., 2010), and it has been suggested that such plasticity contributes to the invasion success of alien plants (Ri chards et aI., 2006). Globally widespread alien species may exhibit high plasticity in physiological and morphological traits that contribute to the maintenance of plant performance under varying amounts of resources (Richards et aI., 2006).
Alternatively, successful species may exhibit plastic responses to
increased resource availability that result in a higher plant performance in high-resource environments, whereas less successful alien or native co-occurring species are less plastic, and are thus less able to increase performance in high-resource environments (Richards et aI., 2006). This second scenario might be a mechanism underlying the theory of fluctuating resource availability and invasibility (Davis et al., 2000), which suggests that the apparently idiosyncratic nature of invasion events results from a requirement of increased resource availability coinciding with invading propagule input.
In addition to biological invasions, increases in resource avail- ability through habitat disturbance and eutrophication (e.g.
atmospheric nitrogen deposition) are major elements of global environmental change (Sala et aI., 2000). It is possible that such increases in resource availability have been to the advantage of those alien, as well as native, species that can capitalize on extra resources. Such potential synergisms between elements of global change may have significant future implications for the extent of floral homogenization worldwide (Dukes & Mooney, 1999;
Bradley et aI., 2010), if widespread alien species are able to
further exploit such resource increases.
Several studies have tested experimentally how invasive plant species respond to changes in resource availability relative to
native species (Funk, 2008; Funk & Zachary, 2010) or non- invasive alien species (Burns, 2004; Hastwell & Panetta, 2005;
Schlaepfer et aI., 2010). Such studies are at a local scale and consider several species, and in order to build wider generaliza- tions the results of such studies can be combined in a quantitative meta-analysis (Davidson et aI., 2011; Palacio-Lopez & Gianoli, 2011). However, many studies have been conducted that are not necessarily focused on invasions, and assess the responses of various plant species to increased availability of resources such as light (e.g. Reich et aI., 1998), nutrients (e.g. James, 2008) and water (e.g. Sack & Grubb, 2002). Such studies offer a valuable opportunity to assess whether more widespread alien plant species tend to be better than less widespread species in general at 859 First publ. in: New Phytologist ; 194 (2012), 3. - S. 859-867
DOI : 10.1111/j.1469-8137.2012.04104.x
Konstanzer Online-Publikations-System (KOPS) URN: http://nbn-resolving.de/urn:nbn:de:bsz:352-217305
maintaInIng plant performance when resources are low, or at increasing performance when resource availability is high, and whether they differ in plastic responses of functional traits, such as SLA and root : shoot ratio. Moreover, use of data from studies that did not focus on invasions per se should minimize the potential for bias toward including only well-known or intensively studied invasive species that have been observed to become dominant after changes in resource availability in the field.
In this study, we employed a meta-analytical approach to test, across many studies and three resource types (nutrients, water and light), whether widespread alien plant species respond more strongly to increased resource availability than do less widespread species. Biomass offers the most direct measure of plant perfor- mance as a product of growth, and thus change in biomass should also offer the clearest indicator of a plant's ability to respond to and take advantage of increased resource availability.
In this study, we combined published data on responses of bio- mass, root: shoot ratio and SLA of plant species to increased resource availability and a global measure of alien species distri- bution (Randall, 2002). Specifically, we asked whether:
• widespread species exhibit a greater increase in biomass in response to higher resource availability (nutrients, water and light) than do less widespread species;
• widespread species change root: shoot ratios to a greater extent than less widespread species in response to increased avail- ability of below-ground resources (water and nutrients). Based on resource-allocation theoty (Bloom et aI., 1985), we might expect that widespread species are better able to reduce root: shoot ratios in response to an increase in availability of below-ground resources, in order to adjust biomass allocation toward capture of light;
• widespread species decrease SLA to a greater degree than less widespread species in response to an increase in light availability.
A greater reduction in SLA in high-light conditions would maintain a high photosynthetic capacity, while minimizing water loss, and thus allow for higher biomass production (Lusk et aI., 2008).
Whilst two other meta-analyses have recently compared trait responses to increased resources of invasive, noninvasive and native species (Davidson et aI., 2011; Palacio-Lopez & Gianoli, 201l), our study is novel for three important reasons. First, we do not restrict our included studies and effect sizes to studies which focused on invasive species, allowing a larger number of effect sizes and species to be considered. Secondly, Palacio-Lopez
& Gianoli (201l) combined effect sizes of different traits together in the same analysis. However, there is no reason to expect success of species to be related to responses of all traits in the same way. Thirdly, we also incorporate phylogenetic structure in our analyses, as species more closely related to one another may respond more similarly to changes in availability of resources than species that are more distantly related to one another. Failure to consider the potential for phylogenetic non independence in such analyses could result in concluding that a significant relationship exists between responses to resource availability and global success when it is actually confounded by phylogenetic history.
Materials and Methods
Study and data collection
We executed a systematic search for data from existing studies published from 1990 to 2009 to obtain as many experimental studies as possible which had manipulated availabilities of light, nutrient or water received by plants, or some combination of the three resource types. Our search for studies was conducted using ISI Web of Science, and we entered as search terms all combina- tions of 'light' I' shade' I' nutrien t*'I' nitrogen' I' drought' I'water' and 'plant phenotypic plasticity'I'plastic*'l'trait*'I'biomass'l 'SLA'I'specific leaf area'I'root: shoot ratio'. Once lists of potential studies had been compiled, we checked the text and figures of each study for evidence that the study involved a manipulative experiment (e.g. glasshouse study, application of resource treatment to planted plants), and for data on biomass (including above-ground only), root: shoot ratio and SLA responses to resource manipulation. We only included studies that reduced the likelihood of confounding resource availability treatments with genetic differences (i.e. studies using replicates of clones, half sibs or seed families in each resource treatment, and/or studies explicitly stating a randomized designation of treatments).
A total of 182 studies met these criteria, covering 347 species and yielding 547 treatment effect sizes. We extracted means, standard deviations and sample sizes of plant biomass, SLA and root: shoot ratio measures under a low-resource treatment and a high-resource treatment where available. We extracted the data from tables, from the main text or from graphs using the program ImageTool (University of Texas Health Centre, San Antonio, TX, USA). When studies had imposed more than two availabilities of a resource treatment, we took biomass in the low- est resource availability and the highest resource availability as 'Iow' and 'high' treatments, respectively. When studies had manipulated more than one resource type in an experiment, we always used the trait measures corresponding to manipulation of the target resoutce, when other resource types were highest and thus unlikely to be limiting. When experimental treatments had been applied to more than one population of a species, we extracted individual trait measures per population. We also recorded the type of resource manipulated (light, nutrients or water). Light manipulations involved shading, lighting, or manipulation of real canopies. Nutrient manipulations involved N, NP, NPK or organic materiaVsoil addition. Water manipula- tions involved reduced provision of water as the 'Iow' resource treatment. We recorded the amount of the resource applied in the low- and high-resource treatments when available. For nutri- ents, we obtained the nitrogen concentration under nutrient manipulation treatments when NP or NPK or soiVorganic matter were applied. We then calculated the magnitude of resource availability difference as the high-treatment amount divided by the low-treatment amount. Where available, we also extracted the duration of the experiment conducted (in d).
From the mean and standard deviations of trait measures and their sample sizes, we calculated each effect size as a log-response
ratio and an associated variance following Rosenberg et al.
(2000), with the Iow resource availability trait measure acting as 'control', and the high resource availability acting as 'treatment'.
Thus, each species (or population within a species) within a study with a specific resource manipulation had an effect size represent- ing the ratio of change in biomass, root : shoot ratio or SLA from a Iow to a high resource availability. A positive effect size would indicate an increase in the value of a trait, whilst a negative effect size would represent a decrease in the value of a trait.
Global distribution of alien species
Because the species from our study search have native ranges spread across the globe, we needed to use a global measure of dis- tribution that integrates records of species present and established throughout their introduced ranges. We achieved this by using the Global Compendium of Weeds (GCW; Randall, 2002), which has also been successfully used in other recent studies (Pysek et aI., 2009; Dawson et al., 2011; Jenkins & Keller, 2011). The GCW represents the most extensive compilation of invasive plant and weed species, incorporating 284 list references with global coverage, and cites> 18 000 taxa between them as being weedy, naturalized or invasive. Every species listed in the GCW is cited in at least one list reference as being in at least one of the above categories. Whilst the GCW is not 100% exhaustive, it provides the best indication to date of how globally widespread alien plant species are known to be, and allows comparison of species native to and introduced to different regions.
We derived a global measure of distribution from the GCW by first counting the number of list references within which a species was cited as 'alien', 'introduced', 'cultivation escape' or 'garden escape', 'naturalized', 'noxious weed', 'sleeper weed' or 'environ- mental weed'. Species listed in only one reference as a 'weed' were not included, as they may have only been recognized as weeds in the native ranges. From these references, we counted the number of global regions within which species were recorded. There were 11 regions in total (also see Dawson et aI., 2011): North America, South America, Central America (including the Caribbean), Europe, Africa, Middle East, South Asia (Bangladesh, Pakistan and India, and Sri Lanka), Eastern Asia (China, Taiwan, Japan, Nepal and Mongolia), Southeast Asia, Australasia and the Pacific Islands (including Hawai'i). It is difficult to discern whether or not species are truly invasive in all regions listed by the GCW.
However, for species in our dataset, the number of global regions is well correlated with the number of states and provinces in North America where a species is naturalized (Spearman's p = 0.533, P < 0.001, number of species = 134; North American data obtained from the United States Department of Agriculture (USDA) plant database, http://plants.usda.gov/java/).This North American distribution database has often been used as a proxy for invasiveness (Mitchell & Power, 2003; van Kleunen & Johnson, 2007). Thus, we believe the GCW represents a reasonable esti- mate of the extent to which alien species are established globally (i.e. they are not just introduced and under cultivation).
Out of the 347 species and 574 effect sizes covered by the resource-manipulation studies, there were 198 species (309 effect
sizes) occurring in the GCW, which had sufficient data on resource manipulation and study duration. Species not occurring in the GCW may not have been widely introduced and cultivated outside of native ranges, or they may be noninvasive despite introduction. To distinguish these two groups of species, we checked for species records in the Germplasm Resources Infor- mation Network (GRIN) taxonomy online database (USDA ARS National Genetic Resources Program, 2010), and if the species was recorded there as cultivated, widely cultivated or naturalized, we included it in the final dataset. This yielded 13 species that were widely cultivated or recorded as naturalized but were not listed in the GCW, giving a total of 211 species (and 332 individual effect sizes) in the final dataset overall, across 129 studies (see Supporting Information, Methods S1). The extra 13 species were recorded as being in zero GCW regions. Most stud- ies and species involved manipulation of nutrient availability (Table 1). Biomass responses were obtained for 149 species, whilst root: shoot ratio responses were obtained for 77 species, and SLA responses for 104 species (Table 1). The majority of species across all data sets were shrubs and trees, and forbs (Table 1). Most species were native to Eurasia and Africa (Table 1). Species with biomass and root: shoot ratio response effect sizes were represented mostly by forb and shrub/tree growth forms, and less by graminoids; species with SLA responses were mostly shrub and tree species (Table 1).
Analysis
In the analysis of the data we have to take into account two important features. First, we are dealing with a meta-analysis (Gurevitch & Hedges, 1999). Secondly, our data points are related to species, and thus we have to take account of potential phylogenetic correlation, that is, the nonindependence of the data points induced by their common history (Felsenstein, 1985). The meta-analyses were conducted using the usual recom- mendations (Gurevitch & Hedges, 1999) to take into account the between-effect size variance and the within-effect size vari- ance. We weighted the data using the inverse of the within-effect size variance plus the estimation of between-effect size variance.
For details about the computations, see chapters 16 and 20 of Borenstein et al. (2009).
The correlation induced by the phylogeny was incorporated into the analyses using phylogenetic regression (Grafen, 1989) with Pagel's lambda correlation structure (Freckleton et al., 2002). This involves using a parameter called lambda to adjust the strength of the correlation induced by Brownian motion, that is, the correlation between two species is given by lambda multi- plied by the fraction of common time length on the phylogenetic tree. The higher lambda is, the greater the strength of the phylo- genetic signal in the residuals; a lambda equal to zero implies that there is no phylogenetic correlation and a lambda equal to one is equivalent to a Brownian motion model. The construction of the phylogenetic trees was done using the online program Phylo- matic (Webb & Donoghue, 2005), and additional published phylogenies were used to resolve polytomies as much as possible (see Methods S2 for details).
Table 1 Summary of the number of studies and species for which effect sizes of plant-trait responses to increased resource availability could be extracted
Biomass R:S SLA
Light Nutrient Water Overall Water Nutrient Overall Light
Studies 40 20 39 90 31 9 39 56
Effect sizes 74 62 92 228 85 37 122 113
Species 64 54 60 149 45 34 77 104
Growth form (species)
Graminoid 8 14 11 28 9 2 10 6
Forb 25 31 17 66 7 28 34 30
Liana 2 2 3 1 4
Shrub/tree 29 9 30 52 29 4 32 64
Origin (species)
Africa 2 3 5 3 3 2
Asia 8 3 9 17 9 10 19
Australasia 1 1 3 1 2 3
Europe 3 2 6 1 3 4 5
North America 3 3 4 10 3 2 5 13
South America 7 3 2 9 2 2 7
Eurasia 12 14 6 27 5 10 15 12
Africa + Eurasia 19 23 22 51 15 15 29 24
North + South America 2 2 4 1 1 7
DisjuncV cosmopolitan 9 2 10 17 5 2 6 12
R : S. root: shoot ratio; SLA. specific leaf area. Also shown are the numbers of species of different growth forms and with different geographic origins represented by effect sizes of biomass. R : Sand SLA responses overall. and for each manipulated resource type.
For analysis ofbiomass responses, we included effect sizes from studies manipulating nutrient, water and light availability. For analysis of root: shoot ratio responses, we only included effect sizes from studies manipulating nutrient and water availability, because root: shoot ratio is a trait commonly measured in relation to uptake of below-ground resources. For analysis of SLA responses, on the other hand, we only included effect sizes from studies manipulating light, because SLA is a trait related to light capture and photosynthetic capacity (Wright et aI., 2004). Moreover, for both root: shoot ratio and SLA, there were vety few studies available for responses to changes in other resources.
Because in a meta-analytical context, the effect size has to be included as the dependent variable, we included our global distri- bution measure as an explanatory variable. This approach has the additional benefit that it allowed us to include other covariates in the models that represented important differences between studies in their methodology, which may affect the magnitude of effect sizes observed. Moreover, it also facilitated inclusion of a phylogenetic structure in our models. To test whether the trait responses depended on the resource type manipulated (nutrients, water or light), we included it as a categorical variable for biomass and root: shoot ratio responses (SLA had only one resource type). Because it is likely that the response of a trait increases with the magnitude of increase in resource availability, we included the magnitude of resource increase (the natural log of the high resource availability divided by the low resource availability) as a covariate. We also included duration of the study (natural-log transformed number of d) as a covariate. These two covariates and our measure of global distribution were scaled to their respective means and standard deviations to allow direct compari- sons of model parameter estimates. For biomass and root : shoot
ratio responses, we ran two separate models: one including an interaction term between resource type and global distribution, and a second without interactions between these two variables.
This allowed us to assess the relationship between global distribu- tion and species responses to resource increases across resource types, and the relationship between global success and species responses depending on the resource type.
The fit of the models was achieved within a Bayesian frame- work under R (R Development Core Team, 2009), and the phylogenies were manipulated using the R package 'ape' (Paradis et aI., 2004). We chose noninformative priors and the sampling of the posterior distribution was done using Monte Carlo Markov chains (burn-in of 5000, sampling of 300 000) (Gilks et aI., 1996). The estimated values of the parameters were computed as the mean value of their corresponding chains, and we used the empirical confidence interval (at 95%) as an estimate of the confidence intervals.
Results
Biomass responses to increased availability of resources Biomass responses were significantly positive for all three resource types on average (Fig. 1a,b). Biomass responses did not significantly differ, on average, between the three resource types (Fig. 1a,b). As the difference between control and treatment resource availability increased ('resource increase'), the magni- tude ofbiomass responses also significantly increased (Fig. la,b).
The parameter estimate for the resource increase effect did not significantly differ between resource types, but the effect of increasing water availability on biomass responses tended to be smaller than increasing nutrient or light availability (Fig. 1a,b).
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Fig. 1 The means (circles) and 95 % confidence intervals (bars) of para- meter estimates describing the relationships between biomass response to increased resources and global distribution of alien species (number of regions), including: (a) interaction between number of regions and resource type; and (b) only main effects for number of regions and resource type. Positive estimates indicate an increase in biomass with increased resource availability for resource type (i.e. intercepts for light, nutrients and water), or a positive relationship between the magnitude of biomass increase and a continuous variable (amount of resource increase per resource type, study length (d), number of regions). Pagel's lambda with 95 % confidence intervals is also given. The dotted line indicates an estimate of zero.
Study duration was not significantly related to the magnitude of biomass response (Fig. la,b). When our measure of species suc- cess (number of global regions) was allowed to interact with resource type in the model, biomass responses to increased resource availability were not significantly related to species suc- cess, for light, nutrients or water (Fig. la). However, across all three resource. types (i.e. without an interaction between species success and resource type), biomass responses of species were significantly and positively associated with the number of global regions where a species was established (Fig. 1 b). Pagel's lambda was low in both models, indicating there was little correlation structure induced by the phylogeny in the residuals of biomass
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Fig. 2 The mean (circles) and 95% confidence intervals (bars) of para- meter estimates describing the relationships between root: shoot ratio response to increased resources and global distribution of alien species (number of regions), including: (a) interaction between number of regions and resource type; and (b) only main effects for number of regions and resource type. Positive estimates indicate an increase in root: shoot ratio with increased resource availability for resource type (i.e. intercepts for nutrients and water), or a positive relationship between the magnitude of root: shoot ratio increase and a continuous variable (amount of resource increase per resource type, study length (d), number of regions). Negative estimates indicate a decrease in root: shoot ratio. Pagel's lambda with 95 % confidence intervals is also given. The dotted line indicates an estimate of zero.
responses, that is, there was almost no phylogenetic signal in bio- mass responses to increased resource availability and the number of global regions.
Root: shoot ratio responses to increased availability of below-ground resources
The intercepts for R : S responses to increased nutrient and water availability were not significantly different from zero, suggesting that, on average, R : S ratios did not significantly change with increased nutrient or water availability (Fig. 2a,b). In addition, R : S responses also did not significantly change with increasing
differences in resource availability between control and treatment (Fig. 2a,b). The variation in root: shoot ratio responses to increased water and nutrient availabilities was large (see 95%
credible intervals in Fig. 2a,b), indicating that biomass allocation shifts under changing resource availabilities are likely to be species-specific.
Study duration was significantly and positively related to the degree of R : S response. As the intercepts did not significantly differ from zero, this indicates that with increasing time, the reduction in R : S in response to increased resource availability becomes smaller (the R : S of control and treatment plants con- verge with increasing experiment duration). The response of R : S to increased resource availability was not significantly related to the number of global regions occupied, for either nutrient increase or water increase (Fig. 2a). There was also no significant relationship between the number of global regions and R: S responses overall (Fig. 2b). The value for lambda was close to one (Fig. 2a,b), indicating that changes in root: shoot ratios with increased resource availability were strongly associated with evolutionary history.
SLA responses to increased availability of light
The intercept of SLA response was significantly negative, indicating, as expected, that across studies and species, increased light intensities led to a decrease in SLA. As the magnitude of resource increase from control to treatment plants grew larger, the magni- tude of SLA reduction also increased, as indicated by the signifi- cantly negative parameter estimate for resource increase (Fig. 3).
Responses of SLA to increased light availability were not signifi- cantly related to the number of regions occupied by a species, or to the duration of the study (Fig. 3). PageI's lambda was very
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Fig. 3 The means (circles) and 95% confidence intervals (bars) of parameter estimates describing the relationships between specific leaf area (SLA) response to increased light intensities and global distribution of alien species (number of regions), and the covariates; amount of resource increase and study length (d). The intercept represents the mean effect size (at average values for other scaled, continuous variables). The negative estimate for the intercept indicates a decrease in SLA with increased light availability. The negative estimate for amount of resource increase indicates a greater SLA decrease with increasing light availability. Pagel's lambda was very close to zero. The dotted line indicates an estimate of zero.
close to zero, suggesting that there was almost no phylogenetic signal in SLA responses to increased light availability.
Discussion
Recently, increasing theoretical attention has been paid to the potential role of phenotypic plasticity in species traits in facilitat- ing the spread of invasive alien species by maintaining plant per- formance under varying environmental conditions, or through allowing species to maximize performance when resource avail- ability is increased (Richards et al., 2006). The. results of our meta-analysis of large numbers of studies manipulating resources for single or few species suggest that species that are more glob- ally widespread are better at capitalizing on increased resource availability, when light, nutrients and water are considered together. Thus, among alien plants, globally successful species are not those best able to maintain plant performance in varied envi- ronments, but tend to be those that are best able to utilize the increases in resource availability that typifY human-disturbed habitats worldwide (Richards et al., 2006; Pysek & Richardson, 2007). The lack of a significant relationship between biomass responses and global distribution when resources are considered separately may reflect lower statistical power, as the trends all tended to be positive. Our results support those of Davidson et al. (2011), who found that when studies compared invasive alien plant species with native species, the alien species tended to be more plastic in their biomass responses to increased resource availability than the native species. Gonzalez et al. (2010) also found that invasive plant species increased performance and growth rate to a greater extent than native species, under increased nutrient availability. For this response to be a true advantage, globally successful alien species should also be more responsive to increased resources than less successful alien species (van Kleunen et al., 2010), and our findings indicate that this is likely to be the case.
Our results may also corroborate the theory of fluctuating resource availability and invasibility, if invasion depends upon alien species responding strongly to increased resource availabil- ity. Davis et al. (2000) suggested that species are only able to colonize and establish in a community if resource availability increases, either through resource input or by reduced resource uptake by the community. An extension of this theory is that species better able to use an increase in resource availability may be more successful at establishing than those that are less able to respond. Leishman & ThomsOl1 (2005) found that increases in nutrient availability were crucial in allowing invasive alien plants to establish over Iow-fertility adapted natives in areas of distur- bance with big increases in water availability, but with inherently Iow fertility. It is unclear from our study whether globally suc- cessful species tend to establish in open, disturbed habitats with low amounts of competition, or whether they are also able to establish in less disturbed, competitive communities when resource availabilities are increased. Many studies in our analyses did not test the responses of species to resource increase in a com- munity context, which would be a prerequisite for testing both the theory of fluctuating resource availability and the hypothesis
that greater alien responses increase the likelihood of the alien invading a community. We cannot rule out the possibility that globally distributed species are merely those best suited to estab- lishing in open, anthropogenically altered habitats, which also tend to have elevated amounts of resources. Thus, the global dis- tributions of successful species may simply reflect the worldwide distribution of similarly disturbed, resource-enriched environ- ments.
In less disturbed habitats, the importance of an increase in resources for establishment of alien plants is likely to vary, depending on how historically limiting the resources in question are at a particular location (Davis & Pelsor, 2001), and on how the recipient community responds to increased resource availabil- ity relative to incoming aliens. Increased availability of a limiting resource is only likely to reduce the amount of competition and community resistance if growth responses by the community do not result in other resources becoming limited. For example, without adequate disturbance, nutrient additions may increase the competition intensity for light exerted by the resident com- munity (Hautier et al, 2010) in areas where soils are relatively fertile, thus increasing, rather than decreasing, resistance to inva- sion. Moreover, it has recently been argued that factors affecting the ability of alien species to establish may act in concert rather than in isolation, such that patterns of invasion success in relation to single factors alone are not apparent (Blumenthal, 2005).
Local-scale studies that set species' responses to increased resource availability in a community context, and interacting with other factors such as enemy release (Blumenthal et al, 2009), will better elucidate how different responses among species play out in terms of shifts in abundance and dominance of alien and native species in those communities. However, hotwithstanding interactions with resident communities and other biotic and abi- otic factors, our study still indicates that globally successful species tend to be more suited to take advantage of increases in resource availability than less successful species.
Optimal-resource allocation theory (Bloom et al., 1985) pre- dicts that plants should invest biomass into structures that allow for uptake of the most limiting resource. However, we found that plants, on average, did not reduce biomass allocation to roots when below-ground resources increased. This contrasts with the results of Reynolds & D'Antonio (1996) and Poorter et al.
(2012), who showed that root mass ratios across multiple species decreased on average in response to increased nutrient availabil- ity. Moreover, there was no relationship between root: shoot ratio responses to increased resource availability and global distri- bution. This corroborates further the findings of Reynolds &
D'Antonio (1996), and more recently Poorter et al. (2012), in that species best suited to high-nutrient environments did not alter their root mass ratios in response to increased nutrient avail- ability compared to species from Iow-nutrient environments.
However, Davidson et al. (2011) found that invasive alien species tended to be more plastic in root: shoot ratio responses to
increased resource availability than native species. Whilst aliens may be better than neighbouring natives at shifting biomass allocation from roots ro shoots under more favourable resource availability (Davidson et al., 2011), our results suggest that at a
global scale an ability to change biomass allocation may not offer a consistent advantage to alien species.
In line with expectations of adaptive shade-tolerance plasticity (Valladares & Niinemets, 2008), SLA decreased when light avail- ability increased, and this decrease tended to be stronger when the difference in light availability increased between treatment and control plants. However, in contrast to expectations, wide- spread species did not decrease SLA to a greater extent than did less widespread species when light availability was higher. A recent multi-species study, including 14 invasive and noninvasive congeneric pairs of species, also found no difference between invasive and noninvasive species in SLA responses to light (van Kleunen et al., 2011). Similarly, plasticity in SLA did not differ between invasive alien and native species in the meta-analysis by Davidson et al. (2011). This implies that plasticity in the ability of plants to capture more light under both low- and high-light conditions by changing SLA does not necessarily contribute to success at a global scale.
The presence of a relationship between global success and bio- mass responses, but the absence of a relationship with root: shoot ratio and SLA responses is intriguing. The greater biomass increases of more widespread alien species under higher availabil- ity of resources may be the result of changes in resource-capture and physiological traits other than SLA and root : shoot ratio.
Alternatively, the performance of plants in varied environments may not simply be the product of their ability to change individual traits (Funk, 2008), but may involve varied responses by multiple traits (Richards et al., 2006). Moreover, resource-acquisition traits of successfully invading species are o&en dependent on the type of habitat being invaded (Leishman et al., 2010; Tecco et aI., 2010).
Differences (Ordonez et aI., 2010; Godoy et al., 2011) or similar- ities (Leishman et aI., 2010; Tecco et aI., 2010) between aliens and natives may be more important to alien success than differ- ences in the capacity of traits to vary (Godoy et al., 201 1). Alterna- tively, Palacio-Lopez & Gianoli (2011) suggest that establishment success of newly introduced species in wide-ranging environments may be determined more by rapid local adaptation than by plasticity. In any case, direct and consistent correlations between plasticity of single traits and plant performance or global success seem increasingly unlikely. Focusing on the endpoint of trait plastici ty - the performance or fitness of the plant under different environmental conditions - is perhaps a more useful approach to understanding whether or not globally widespread or invasive species are successful owing to their ability to survive and out- perform other species in multiple environments.
In summary, our study suggests that the ability of plant species to increase biomass in response to increased resource availability also appears to confer species success at a global scale, but that plasticities of individual resource-capture traits are unlikely to be consistently related to species success. The search for a relation- ship between plasticity of individual traits and species success may be less fruitful than measuring plant performance under dif- ferent environments. Whether an ability to increase biomass translates ultimately to increased individual and population-level fitness for widespread, successful species requires more detailed experiments involving multiple native and alien, successful and
unsuccessful species, grown under different environmental condi- tions and involving direct fitness measurements.
Acknowledgements
This work was funded by the Swiss National Science Foundation in the framework of the Swiss National Centre for Competence in Research 'Plant Survival'. R.P.R. was also partially supported by funding from FP7-REGPOT 2010-1, grant no. 264125 EcoGenes.
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Supporting Information
Additional supporting information may be found in the online version of this article.
Methods SI List of studies from which data were extracted.
Methods S2 Methods for constructing phylogenetic trees, and trees used.
